Greenhouse Evaluation of Capsicum Accessions for Resistance to European Corn Borer (Ostrinia Nubilalis)

HORTSCIENCE 39(6):1336–1338. 2004. mendations for ECB include locating pepper fi elds away from corn fi elds, plowing down crop residue to destroy over-wintering larvae, Greenhouse Evaluation of Capsicum and clearing fi eld perimeters of weedy habitat. However, growers face stringent standards Accessions for Resistance to European regarding ECB contamination, and rejection of processing pepper lots is common at infestation Corn Borer (Ostrinia nubilalis) levels as low as 5% to 10%. Thus, there is a very low tolerance for corn borer in pepper fi elds, and James D. Frantz weekly insecticide applications are recommended Department of Plant Breeding, Cornell University, Ithaca, NY 14853 to protect fruit from the onset of second fl ight moth activity until harvest. Heavy dependence Jeffrey Gardner and Michael P. Hoffmann on regular insecticide use for control of ECB in Department of Entomology, Cornell University, Ithaca, NY 14853 pepper is expensive and poses risks in terms of toxicity, development of resistance in the pest Molly M. Jahn1 and shifting regulatory restrictions on pesticides Department of Plant Breeding, Cornell University, Ithaca, NY 14853 registered for use in vegetable crops. Genetic resistance to ECB in commercial Additional index words. insect resistance, pepper, pungency, vegetable breeding, integrated pepper varieties could help alleviate some of pest management these problems. There is a great deal of vari- ability in Capsicum with regard to response to Abstract. A replicated greenhouse evaluation of a range of commercial and noncommercial ECB damage, largely associated with pungency (Capsicum spp.) accessions for resistance to european corn borer (ECB) [Ostrinia nubilalis level. Two studies have reported ECB resistance (Hubner)] was conducted. Percentage of fruit damaged was observed among 29 accessions evaluations in pepper. Jarvis and Guthrie (1972) four weeks after plants were artifi cially infested with ECB egg masses. Small-fruited peppers evaluated 120 Capsicum plant introductions generally showed lower levels of damage, while large-fruited peppers were the most susceptible. and 4 cultivars for resistance to corn borer Genotypes with elongate fruit were less damaged than those with bell-shaped fruit. Resistance infestation. They examined susceptibility to to fruit damage was also associated with increasing pungency level, with two notable excep- ECB damage with respect to commercial type, tions. The pungent genotype ‘Large Red Thick Cayenne’ was signifi cantly more susceptible fruit shape, fruit size, and pungency level. Their than many of the other pungent accessions tested. The relative susceptibility of this accession results indicated that pimento and bell were may be related to large fruit size. The nonpungent pepper ‘Corno di Toro’ showed signifi cantly the most susceptible market types, followed lower percent fruit damage than other nonpungent peppers including ‘Banana Supreme’ by paprika, chile, cayenne, tabasco, and orna- with roughly similar fruit size, ranking amidst highly pungent peppers such as ‘Red Scotch mental. Genotypes with bell and conical fruit Bonnet’. These results confi rm that resistance to ECB can be identifi ed in nonpungent Cap- shapes were the most susceptible, followed by sicum genotypes and demonstrate that pungency is not always correlated with ECB damage. elongate, round, and oblate. Larger pods were Reported sources of aphid resistance or tolerance showed good levels of ECB resistance, but more susceptible to damage than smaller pods. interpretation of these results was confounded by the presence of pungency. Nonpungent peppers were the most damaged, The european corn borer (ECB) has an small amount of sawdust-like frass as the only followed by pungent and very pungent peppers. extremely wide host range, which has resulted indication of fruit infestation. ECB develop An accompanying feeding study demonstrated in its status as a signifi cant pest of many dif- through fi ve larval instars before they pupate that even low concentrations of capsaicin were ferent agronomic and vegetable crops. Since and become adults; a process which in maize is effective in reducing larval growth and develop- being introduced from Europe in the early ≈30 d in duration. Within infested pepper fruit, ment. The authors concluded that capsaicin was 1900s, ECB has spread to all but the seven most fi rst and second larval instars feed primarily on an important factor determining resistance. A western states of the continental U.S. In many calyx and placental tissues, while later instars later study compared ECB damage among two parts of its host range, ECB has become the continue development in the primary fruit or commercial nonpungent peppers and six breed- most important insect pest of peppers, including move to bore into secondary fruit or stems. ing lines after artifi cial infestation. Resistance vegetable growing regions of New York , New Wounds produced by ECB entry holes promote was once again associated with pungency, England, the Midwest and southern Canada. bacterial infection of the fruit by Erwinia caro- although one nonpungent pepper breeding line In New York, all pepper acreage is annually tovora. As fruit progressively deteriorate due showed a fair level of resistance compared to affected by ECB, with up to 50% yield losses to soft rot, larvae move into uninfected fruit, commercial bell peppers. This breeding line in severely infected fi elds. spreading the disease. In southern New England had smaller fruit, more fruit per plant, smaller The life history of ECB on pepper has and comparable environments, the second fl ight leaves and less compact habit relative to bell pep- been reviewed. While maize is the preferred of bivoltine ECB strains coincides with pepper pers. Feeding studies confi rmed that increasing host for ECB, female moths will also lay eggs fruit set in production fi elds. capsaicin levels reduced larval survival, while on leaves of pepper plants. Economic damage Integrated pest management control recom- reduced survival to pupation was observed after results when oviposition occurs during periods of fruiting, a regular occurence. Larvae hatch Table 1. Sources of Capsicum accessions evaluated for resistance to European corn borer. in 1 to 2 weeks and disperse onto fruit, where they enter by boring under the calyx, leaving a Source and Location Accession Asgrow Seed Co., San Juan Bautista, CA NuMex RNaky Received for publication 6 May 2003. Accepted for AVRDC, Taiwan PBC 18, PBC 30, PBC 84, publication 19 Nov. 2003. We would like to thank PBC 345 (Serrano Vera Cruz), PBC 681 (Early Jalapeno), Margaret Smith for laboratory-produced European PBC 750 (Szeged 40017), PBC 1351 corn borer egg masses and the Asian Vegetable CalCompack Foods, King City, CA CalCompack Research and Development Center for cotton aphid Cornell University, Ithaca, NY (T. Thorup) Red Scotch Bonnet resistant germplasm. This study was funded in part by INRA, France Perennial the Cornell University Vegetable Breeding Institute, Stokes Seeds, Buffalo, NY Ace, Camelot, Merlin a consortium of companies that support plant breed- Tomato Growers Supply Co., Fort Myers, FL Banana Supreme, Big Bertha, Commandant, ing research at Cornell, along with funding from Corno di Toro, Gypsy, Large Red Thick Cayenne, USDA IFAFS Award No. 2001-52100-11347. NuMex Joe E. Parker, Paprika Supreme, 1To whom reprint requests should be addressed; Pasilla Bajio, Pepperoncini, Peto Wonder, Pimento L, e-mail [email protected]. Serrano, Super Cayenne II, Super Red Pimento

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77739-Pest.indd739-Pest.indd 11336336 99/20/04/20/04 112:02:032:02:03 PPMM feeding larvae a diet containing 20% ground sizes for resistance to ECB damage, both to (Premier ProMix, Dorval, Quebec) and grown fruit from the most resistant pungent accessions confi rm the general relationship of these traits under halogen lights in the Cornell University when compared to similar treatment using a to resistance and to see if ECB resistance could Insectary greenhouse. Six-week-old seedlings nonpungent pepper breeding line. be recovered in nonpungent genotypes. were transplanted on 2 June into 200-mm pots Although resistance to ECB has been linked (Kord Products, Toronto, Ont.) and grown in to capsaicin content, pungency is clearly undesir- Materials and methods the greenhouse without supplemental lighting. able in nonpungent peppers, therefore potential Greenhouse temperatures were maintained be- sources of resistance are required that are in- Plant materials and market types. Sources tween 22 and 32 °C. Plants were fertilized with dependent of pungency. One strategy to locate of pepper germplasm evaluated in this study Peters 20–20–20 plant food (Scotts, Marysville, useful germplasm is to search accessions with are listed in Table 1. Market types used in Ohio) once every week. tolerance or resistance to other insect pests. Pepper this study are as follows. Ornamental pep- ECB infestation and damage evaluation. accessions that have been identifi ed for resistance pers (C. annuum) are small-fruited, generally The evaluation study was arranged as a ran- or tolerance to cotton aphid (CA) infestation thin-fl eshed, and pungent. Chili peppers (C. domized complete block design with one plant could potentially provide pleiotropic resistance annuum) are elongate, thick-fl eshed, and pun- per replication and six replications. Each block to ECB. Precedence for this has been noted in gent. Aji peppers (C. baccatum) are elongate, consisted of a greenhouse bench with plants ar- maize with resistance to both corn leaf aphid and thin-fl eshed, and pungent. Caribbean peppers ranged 33 cm inches apart within rows and 54 ECB leaf feeding associated with the presence of (C. chinense) are blocky, thin-fl eshed, and ex- cm between rows. Plants were infested on two the hydroxamic acid DIMBOA [2,4-dihydroxy- tremely pungent. Pasilla peppers (C. annuum) dates, 16 and 25 Aug., after most accessions 7-methoxy-(2H)-1,4-benzoxazin-3(4H)-one]. In are large, elongate, and thin-fl eshed with low had set several fruit. Artifi cial infestation was tomato, resistance to both the nematode Meloido- pungency. Paprika peppers (C. annuum) are accomplished by pinning two ECB egg masses gyne incognita and potato aphid are controlled elongate and thin-fl eshed with low pungency. containing ≈20 eggs each onto stems near fruit. by the Mi gene. Leaf pubescence, in the form of Cayenne peppers (C. annuum) are elongate, Laboratory produced ECB egg masses were glandular trichomes that exude acylsugars, has slightly curved, thin-fl eshed and pungent. Chile provided by M. Smith, Cornell University. Four been associated with resistance to a wide range peppers (C. annuum) are large, elongate pep- weeks after the second infestation, fruit were of pests in tomato including both aphids and pers with thick fl esh and mild pungency. Italian examined for signs of ECB damage. Any fruit lepidopterans. sweet peppers (C. annuum) are large, elongate with signs of ECB damage or presence of larvae One objective of our study was to test an ar- peppers with thick, sweet fl esh. Pepperoncini were counted as infested. ray of pepper accessions with several potentially peppers (C. annuum) are thin-fl eshed, elongate Percentage of fruit infested was determined important characteristics, including those with and mildly pungent. Bell peppers (C. annuum) based on the number of infested fruit out of the resistance to CA, for their relative resistance are nonpungent with thick fl esh and blocky total number of fruit at harvest. Expected survi- to ECB. A second objective was to observe shape with three to four lobes. Pimentos (C. vorship of ECB larvae before boring into maize whether leaf pubescence provides protection annuum) are nonpungent peppers with thick plants is 20% to 50% depending on environmental from ECB damage. The fi nal objective was fl esh and conical or oblate shape. conditions. Given relatively protected conditions to evaluate additional pepper accessions with Plant culture. Plants were seeded on 21 in the greenhouse, expected survivorship to the a range of pungency levels, fruit shapes and Apr. 1999 into commercial peat potting mix boring stage on pepper fruit was set at 50%. Based Table 2. Percentage of fruits damaged among Capsicum accessions artifi cially infested with European corn borer egg masses. Damaged fruit (%) Accession Typez Pungencyy Sizex Shape Rank Mean Perennial Ornamental Pungent Small Elongate 1 0.00 aw PBC 30v Cayenne Pungent Medium Elongate 1 0.00 a PBC 1351 v Aji Pungent Small Elongate 3 0.83 a PBC 18 v Cayenne Pungent Medium Elongate 4 1.85 ab Serrano Chili Pungent Small Elongate 5 2.08 ab Serrano Vera Cruz Chili Pungent Small Elongate 6 2.94 ab Red Scotch Bonnet Caribbean High Medium Blocky 7 4.44 abc Super Cayenne II Cayenne Pungent Medium Elongate 8 8.65 abcd Early Jalapeno v Chili Pungent Medium Elongate 9 9.93 abcd Pasilla Bajio Pasilla Mild Large Elongate 10 16.67 abcde Paprika Supreme Paprika Mild Large Elongate 11 18.71 abcdef Szeged 40017 Paprika Mild Large Elongate 12 21.69 bcdef Corno di Toro Italian sweet Sweet Large Elongate 13 24.20 cdef Large Red Thick Cayenne Cayenne Pungent Large Elongate 14 28.07 defg Cal Compack Paprika Mild Large Elongate 15 32.04 efg NuMex RNaky Chile Mild Large Elongate 16 35.75 efgh NuMex Joe E. Parker Chile Mild Large Elongate 17 37.18 fgh Banana Supreme Italian sweet Sweet Large Elongate 18 46.79 gh Pepperoncini Pepperoncini Mild Medium Elongate 19 52.75 h Gypsy Bell Sweet Large Conical 20 75.13 i PBC 84 v Bell Sweet Large Bell 21 76.39 ij Camelot Bell Sweet Large Bell 22 80.56 ij Commandant Bell Sweet Large Bell 23 82.18 ij Peto Wonder Bell Sweet Large Bell 24 82.78 ij Pimento L Pimento Sweet Large Conical 25 83.47 ij Ace Bell Sweet Large Bell 26 84.26 ij Super Red Pimento Pimento Sweet Large Oblate 27 85.52 ij Merlin Bell Sweet Large Bell 28 87.78 ij Big Bertha Bell Sweet Large Bell 29 95.83 j zSee description of market types in Materials and Methods. yPungency ratings: sweet (no pungency), mild (<1000 Scoville Units), pungent (2000 to 50,000 Scoville Units), high (>100,000 Scoville Units). xSmall = average width <2.5 cm and average length <5 cm, medium = average width 2.5 cm to 5 cm and average length 5 cm to 10 cm, large = average width >5 cm and average length >10 cm. wMean separation by Fisher’s protected LSD test, P = 0.05. vShows tolerance to cotton aphid (Frantz et al., in press).

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77739-Pest.indd739-Pest.indd 11337337 99/20/04/20/04 112:02:052:02:05 PPMM on initial infestation of 80 eggs and expected was not signifi cantly different from the highly trol agents, e.g., parasitoid wasps, or chemical survivorship of 40 larvae per plant, the upper pungent ‘Red Scotch Bonnet’. Mildly pungent agents. Among the highly resistant hot peppers, limit of total fruit (infestable) per plant was ad- accessions Pasilla Bajio, Paprika Supreme and the next step will involve segregation analysis justed to 40 when calculating the percent of fruit Szeged 40017 also performed well, ranking to determine whether there is any independence infested. This adjustment was only required for slightly better than ‘Corno di Toro’. between ECB resistance and pungency. If so, it two plants of ‘Perennial’, four plants of PBC 1351, would open up a much larger germplasm base and one plant of ‘Red Scotch Bonnet’. Analysis Discussion for resistance breeding. of variance and Fisher’s protected LSD test (P= 0.05) was performed using Minitab Version 13 The most pressing need for ECB resistance Literature Cited (Minitab, State College, Pa.). is in highly susceptible bell and pimento types, Ajlan, A.A., D.E. Knavel, and J.G. Rodriguez. 1985. Re- therefore useful resistance sources must be inde- sistance of pepper, Capsicum annuum L. to European Results pendent of pungency. A nonpungent source of corn borer Ostrinia nubilalis (Hubner). Trans. Ky. Acad. reduced damage such as ‘Corno di Toro’ could Sci. 46:99–103. Boucher, J. 1999. Pepper IPM: European corn borer. 5 Ranks, assigned to accessions based on be useful in an attempt to improve levels of Mar. 2003. www.hort.uconn.edu/ipm/veg/htms/ppr- resistance to fruit damage, ranged from the top damage in bell and pimento types. It is possible borer.htm. ranking (1) for ‘Perennial’ and PBC 30 with that reduced damage in this accession could be Campos, F., J. Atkinson, J.T. Arnason, B.J.R. Philogene, P. the least amount of damage (0%) to the lowest related to a character such as a tightly sealed ca- Morand, N.H. Werstiuk, and G. Timmins. 1989. Toxi- cokinetics of 2,4 dihydroxy-7-methoxy-1 4-benzoxazin- ranking (29) for ‘Big Bertha’ with the highest lyx architecture that excludes fi rst instar larvae. 3-one DIMBOA in the European corn borer Ostrinia amount of damage (95.83%) (Table 2). Pungent Based on the fact that we recovered this source in nubilalis Hubner. J. Chem. Ecol. 15:1989–2002. to highly pungent accessions comprised the top an evaluation of a limited number of nonpungent Capinera, J.L. 2001. Handbook of vegetable pests. Academic nine resistance rankings for percent fruit dam- accessions, further evaluation of nonpungent Press, San Diego, Calif. Cornell Cooperative Extension Service. 2002. Integrated age. Mildly pungent peppers comprised 7 out of pepper germplasm could reveal better sources crop and pest management recommendations for com- the next 10 most resistant rankings. The lowest of resistance for breeding programs. Segrega- mercial vegetable production. Cornell Univ. Coop. Ext. ranked ten accessions were all nonpungent. tion analysis of crosses made between ‘Corno Serv., Ithaca, N.Y. Small-fruited accessions comprised four of di Toro’ and highly susceptible peppers will be Cranshaw, W., C. Welty, and R. Bessin. 1995. Peppers and eggplant, p. 89–98. In: R. Foster and B. Flood (eds.). the top six rankings and large-fruited accessions required to determine the mode of inheritance Vegetable insect management with emphasis on the comprised the 19 out of the 20 lowest rankings. and to examine in further detail the relationship Midwest. Meister Publ. Co., Willoughby, Ohio. Elongate shaped peppers comprised 19 of the 20 between thickness of fruit walls, fruit shape and Gardner, J., M.P. Hoffmann, and M.E. Smith. 2000. Resis- top resistance rankings for percentage of fruit other characters with resistance to ECB. tance to european corn borer in processing sweet corn. Hortscience 35:871–874. damaged, while bell shaped peppers comprised The mildly pungent accessions Pasilla Bajio, Goffreda, J.C., M.A. Mutschler, and W.M. Tingey. 1988. 7 out of the 9 lowest ranked accessions. These Paprika Supreme and Szeged 40017 may also Feeding behavior of potato aphid affected by glandu- results are consistent with previous studies. represent possible sources of resistance for lar trichomes of wild tomato. Entomol. Expt. Appl. One of the objectives of the study was to introgression into bell and pimento peppers, if 48:101–108. Gurr, G.M. and D. McGrath. 2002. Foliar pubescence and determine whether resistance to ECB could be the resistance can be introgressed with a minimal resistance to potato moth, Phthorimaea operculella, found among accessions rated resistant to CA. amount of pungency. The surprising level of in Lycopersicon hirsutum. Entomol. Expt. Appl. CA-resistant accessions PBC 30, PBC 1351, susceptibility in pungent genotype‘Large Red 103:35–41. and PBC 18 were three of the four top ranked Thick Cayenne’ may be related to large fruit Hagerman, P. 1997. European corn borer in sweet corn and other horticultural crops. 5 Mar. 2003. www.gov.on.ca/ accessions for percent fruit damage, and the CA- size. It suffered nearly 20% more fruit dam- OMAFRA/english/crops/facts/97-019.htm. tolerant line ‘Early Jalapeno’ was also in the top aged fruit than the medium-sized commercial Hazzard, R.V. 1997. European corn borer management in resistance grouping. All four of these accessions cayenne ‘Super Cayenne II’, and >25% more peppers. 5 Mar. 2003. www.hort.uconn.edu/ipm/veg/ are pungent, therefore ECB resistance in these fruit damage than medium-sized cayenne pep- htms/nmbbrer.htm. Jarvis, J.L. and W.D. Guthrie. 1972. Relation of horticultural accessions cannot be separated from pungency pers PBC 30 and PBC 18. characteristics of peppers to damage by larvae of the without performing segregation analysis by Evaluation of resistance under greenhouse european corn borer. Iowa State J. Sci. 46:463–470. making genetic crosses to nonpungent types. conditions provides a stable environment for Juvik, J.A., J.A. Shapiro, T.E. Young, and M.A. Mutschler. However, the CA-resistant nonpungent bell infestation, but there are clear and possibly signifi - 1994. Acylglucoses for wild tomatoes alter behavior and reduce growth and survival of Helicoverpa zea and pepper PBC 84 was very susceptible to ECB cant phenotypic differences between greenhouse Spodoptera exigua (Lepidoptera: Noctuidae). J. Econ. damage. Assuming that the mechanism of re- and fi eld-grown pepper plants. Field grown plants Entomol. 87:482–492. sistance is consistent among the CA-resistant tend to be more compact with more leaf cover, Long, B.J., G.M. Dunn, J.S. Bowman, and D.G. Routley. 1977. accessions, ECB susceptibility in PBC 84 which could favor dispersal of fi rst instar ECB Relationship of hydroxamic-acid content in corn and resistance to the corn leaf aphid. Crop Sci. 17:55–58. indicates no evidence of pleiotropy between larvae, resulting in higher levels of overall infesta- Mason, C.E., M.E. Rice, D.D. Calvin, J.W. Van Duyn, CA resistance and ECB resistance. tion. On the other hand, in unprotected conditions, W.B. Showers, W.D. Hutchison, J.F. Witkowski, The pubescent pepper accessions ‘Serrano’ predation by natural enemies and losses to abiotic R.A. Higgins, D.W. Onstad, and G.P. Dively. 1996. and ‘Serrano Vera Cruz’ were highly resistant stresses could mitigate ECB infestation pressure. European corn borer: Ecology and management. Iowa State Univ., Ames. to fruit damage, ranking fourth and fi fth overall. Further testing will be required to determine the Robinson, J.F., J.A. Klun, and T.A. Brindley. 1978. European Fruit of these accessions are small and pungent, extent to which results from greenhouse evalua- corn borer: a nonpreference mechanism of leaf feeding so again, further characterization is required tions predict fi eld performance. resistance and its relationship to 1, 4-benzoxazin-3-one to separate the effects of pubescence from the Since there is a very low tolerance for ECB concentration in dent corn tissue. J. Econ. Entomol. 71:461–465. effects of pungency level and fruit size. damage in commercial pepper crops, high levels Rodriguez, A.E., W.M. Tingey, and M.A. Mutschler. 1993. All bell pepper entries evaluated were highly of resistance would be required to curb regular Acylsugars of Lycopersicon pennelli deter settling and susceptible, with >75% infestation. Pimento insecticide use. Further evaluation should con- feeding of the green peach aphid (Homoptera: Aphididae). types were also highly infested, with >80% tinue for resistance to ECB, although the limited J. Econ. Entomol. 86:34-39. Stivers, L. 1999. Crop profi les for peppers of New York. 24 infestation. The Italian sweet types ‘Corno di amount of genetic variability within nonpungent May 2003. www.pestdata.ncsu.edu/cropprofi les/docs/ Toro’ and ‘Banana Supreme’ showed signifi - peppers suggests it may be diffi cult to fi nd highly nypeppers.html. cantly less ECB damage than bell and pimento resistant sources for improvement of bell and Talekar, N.S., and T. Berke. 1998. Breeding for pest resis- types. They grouped instead with other large- pimento accessions. Even an intermediate level tance/tolerance in pepper, p. 165–168. Xth EUCARPIA Meeting on Genetics and Breeding of Capsicum and fruited elongate peppers in the study, most of of resistance, as observed in ‘Corno di Toro’, Eggplant, Avignon, France. which have mild pungency. It is striking that would be useful if it reduced the number of Vos, P., G. Simons, T. Jesse, J. Wijbrandi, L. Heinen, R. ‘Corno di Toro’ was signifi cantly more resistant sprays required to produce a crop. Host plant Hogers, A. Frijters, J. Groenendijk, P. Diergaarde, M. than ‘Banana Supreme’, and actually ranked resistance might be most likely to provide Reijans, O.J. Fierens, M. de Both, J. Peleman, T. Liharska, J. Hontelez, and M. Zabeau. 1998. The tomato Mi-1 gene above the pungent pepper ‘Large Red Thick complementary control of ECB when combined confers resistance to both root-knot nematodes and potato Cayenne’. Fruit damage to ‘Corno di Toro’ with with inoculative releases of biological con- aphids. Nature Biotechnol. 16:1365.

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